Diffuse idiopathic skeletal hyperostosis in Meroitic Nubians from Semna South Sudan.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 92:243-248 (1993) Diffuse Idiopathic Skeletal Hyperostosis in Meroitic Nubians From Semna South, Sudan BERNARD0 T. ARRIAZA, CHARLES F. MERBS, AND BRUCE M. ROTHSCHILD Department of Anthropology and Ethnic Studies, University of Nevada, Las Vegas, Los Vegas, Nevada 89154-5012 and Smithsonian Institution, Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560 (B.T.A.1; Department of Anthropology, Arizona State University, Tempe, Arizona 85287-2402 (C.F.M.1;Arthritis Center of Northeast Ohio, Northeast Ohio Universities, College of Medicine, Youngstown, Ohio 44512 (B.M.R.) KEY WORDS Arthritis, Vertebral column DISH, Forestier’s disease, Aging, ABSTRACT The paleopathological study of human osteological remains from the site of Semna South, of northern Sudan, revealed that about thirteen percent of this ancient Nubian population had diffuse idiopathic skeletal hyperostosis (DISH). As in modern cases, males were more affected than females. Two thousand years ago, ancient Nubian males had the same spinal problems elderly men have today. o 1993 Wiley-Liss, Inc. This paper summarizes paleopathological research undertaken on a Nubian skeletal collection to search for early evidence of diffuse idiopathic skeletal hyperostosis (DISH) in Africa. DISH is a common skeletal abnormality, affecting 20-27% of men over 50 years of age (Forestier and Lagier, 1971; Resnick et al., 1978; Rothschild, 1988; Rothschild and Woods, 1991).DISH does not cripple the individual; thus, some scholars do not consider it a disease, but rather an anomaly of aging or a special skeletal phenomenon (Resnick et al., 1978; Resnick and Niwayama, 1976; Rothschild, 1988). From the systematic clinical studies done by Forestier and Rotes-Querol (1950) and Forestier et al. (1956), the first diagnostic criteria were derived. As Forestier and Rotes-Querol used the term “ankylosing hyperostosis” to designate a specific type of spinal anomaly which was clearly distinct from ankylosing spondylitis, the phenomenon is also referred to as Forestier’s disease or as Forestier and Rotes-Querol disease. DISH has gone by various names in the past (Table 1). In 1975, Resnick and his co-workers coined the term “diffuseidiopathic skele0 1993 WILEY-LISS, INC. tal hyperostosis” (DISH) to emphasize that extra spinal manifestations, enthesis ossifications, are also common. The acronym DISH is currently preferred over ankylosing hyperostosis. MORPHOLOGY OF DISH AND OTHER SPINAL DISEASES The etiology of DISH is unknown. DISH has a distinctive morphology that differentiates it from other rheumatic disorders. DISH is typified by ossification of the anterior longitudinal ligament, especially along the right anterolateral aspect of the thoracic vertebrae (Fig. 1). DISH is easily recognizable in a lateral radiographic view of the spine. The outgrowths appear as a dense and continuous line of bumps, or as a “candle flame.” In the bare bone this condition can be observed as a flowing ossification Received for publication June 25,1992; accepted May 19,1993. Address reprint requests to Dr. Bernard0 T. Arriaza, Department of Anthropology and Ethnic Studies, University of Nevada, Las Vegas, 4505 Maryland Parkway, Las Vegas, Nevada 891545012. B.T. ARRIAZA ET AL. 244 the sacroiliacjoints in DISH are not fused as in ankylosing spondylitis. Individuals with Forestier’s disease DISH keep most of their back flexibility, Ankylosing hyperostosis whereas those with ankylosing spondylitis Moniliform hyperostosis do not. Back flexibility is possible in paHyperostosis of the spine Spondylosis hyperostotica tients with DISH because most anterior SDondvlitis ossificans kamentosa flexion occurs at the lumbar segment and Senile“anky1osinghyper&& of the spine Ankylosing hyperostosis of Forestier and Rotes-Querol DISH typically affects the thoracic segment instead. In contrast, in patients with anky‘After: Resnick e t al. (1978);Utsinger (1984). losing spondylitis, back flexion is restricted due to fusion of the lumbar vertebral bodies and their apophyseal joints. Vertebral squaring, which typifies ankylosing spondylitis, does not occur in DISH (Forestier and Lagier, 1971; Yagan and Khan, 1983). The syndesmophytes of ankylosing spondylitis are thin bridges through the anulus fribosus from one vertebral body to the next, contrasting with the thick longitudinal ossification of DISH. Also, ankylosing spondylitis mainly affects young adults as opposed to the older age of onset in DISH. In both phenomena, the intervertebral space tends to be maintained and both may present “whiskering” of the peripheral joints (Resnick et al., 1978). Reiter’s syndrome and psoriatic arthritis, types of seronegative spondyloarthropathies, may also produce thin or thick paravertebral fusion, but overall this type of fusion parallels ankylosing spondylitis rather than DISH (Rogers et al., 1985). Fluorosis may also cause osteophytosis but periostitis and sclerosis are more typical of fluorosis (Ortner and Putschar, 1985). Ochronosis and induced calcium pyrophosphate depositation disease, metabolic disorders, more closely resemble ankylosing spondylitis rather than DISH. Extensive intervertebral disc ossification is typically present in ochronosis (see Ortner and Putschar, 1985). Fig. 1. Thoracic vertebrae of a Nubian male from the Hypoparathyroidism, hypophosphatemia, Semna South site showing the typical flowing ossification seen in DISH. hypervitaminosis A, and healing fractures are rare phenomena which can mimic DISH (Forestier and Lagier, 1971; Resnick et al., (Fig. 1)sometimes called a “dripping candle 1978). Limitation of the phenomena to Nuwax” pattern (Forestier and Rotes-Querol, bian adults allows hypervitaminosis A to be 1950; Forestier and Lagier, 1971; Resnick ruled out. et al., 1978; Resnick and Niwayama, 1981; MATERIALS AND METHODS Rothschild, 1988). The skeletal remains of 134 adult Meroitic DISH in the past may have been confused with ankylosing spondylitis. The apophy- Nubians from the Semna South site were seal, costovertebral, and auricular surface of examined. The cemetery was excavated in TABLE 1 . Most common synonyms for DISH or Diffuse IdioDathic Skeletal Hwerostosis 245 DISH IN NUBIANS ASWAN HIGH D A M 2' ND C A T A R A C T DAL CATARACT 3 RO CATARACT Meroe MI. 0 I 0 KM. I- 50 I 100 100 I 150 J 200 300 ETHIOPIA, Fig. 2. The Wadi Halfa area of Sudan and surrounding localities (After Van Gerven, 1981). 1966-1968 in Northern Sudan, near the concentrated on the spine only. Sex was inNile region, 15 miles south of Wadi Halfa ferred from the size of the lumbar vertebrae, (Fig. 2). Currently the skeletal remains from sacrum, and femoral head diameter, followSemna South are housed at the Anthropol- ing standard osteological techniques (Krogogy Department of Arizona State Univer- man and Iscan, 1986; Bass, 1987). Because sity. The cultural association of these inhu- DISH is an age-dependent phenomenon, mations corresponds to groups that based only the skeletons of mature adult individutheir economy on agriculture (Meriotic Pe- als were considered in the following analysis riod, 350 B.C. to A.D. 350; Armelagos, 1977; and interpretations. No evidence of DISH Van Gerven, 1981; Zabkar and Zabkar, was noted in younger individuals. 1982). Research model As DISH is a product of aging and as the vertebrae manifest the pathognomonic features of the phenomenon, the present study RESULTS AND DISCUSSION Eighteen cases (13.4%) of DISH were identified among 134 adult Nubian spines (Table 2). Diffuse idiopathic skeletal hyper- B.T.ARRIAZA ET AL. 246 TABLE 2. Specimens diagnosed as having DISH (based on the Dresence o f Forestier’s disease) Females (n = 56) SDecimen Condition N235 N236-1 N268 N 408-2 DISH DISH DISH DISH + SNS Males (n = 78) SDecimen Condition N 201 N 228B N 244 N 270 N 271 N 277 N 282 N 296-1 N 410 N 413 N 414 N 422-1 N 448-2 N 521 DISH DISH DISH DISH DISH DISH DISH + SNS DISH DISH DISH DISH DISH DISH + SNS DISH ostosis was found in 7% of the females while males had 18%(Chi square = 3.3, P> 0.05). Two males and one female had associated seronegative spondyloarthropathies (SNS), diagnosis based on the presence of irregular and bulky vertebral ankylosing, apophyseal fusion and periarticular erosions. Given the high population frequency of DISH in this Nubian sample, seronegative spondyloarthropathies could be anticipated to co-occur in this population. DISH in Nubians The present study of Nubians shows DISH was present in Africa as early as the third century B.C. A 13.4% frequency of DISH in these adult Nubians is high compared to other archaeological studies from other areas, but lower than some modern populations. Perhaps this high DISH prevalence in Nubians is due to sample bias during excavation or recovery. Although the authors were not involved in the excavation of the Semna South site, to the best of our knowledge the Nubian skeletons analyzed represents a random sample. Arriaza (1993) found 4% DISH in an approximately 4,000year-old sedentary fishing population from northern Chile. Rogers et al. (1985)reported a frequency of 2-3.7% DISH in a study of Egyptian and European skeletons dating from the twenty-first dynasty through A.D. 1850. For the Middle Ages, DISH has been found to be as common (Kramar et al., 1990; Waldron, 1985) as it is today for modern European populations. Using clinical data, Julkunen et al. (1971,1975) reported a 3.8% and 2.6% occurrence of DISH for modern Finnish men and women over 40 years of age, respectively. However, the frequencies increased to 10% in individuals over 70 years of age. Rothschild and Woods (1991) using the Todd collection (Cleveland Museum of Natural History) found DISH in 25% of men over age 65 while women had only 4%. There are three points about DISH which have special anthropological importance: (1) typically there is a late age of onset for DISH; (2) there is differential sex distribution, with greater numbers of males affected; and (3) DISH has been associated with high caloric intake, although this has not been confirmed. These observations, when related to the evidence of DISH in this Nubian population, raise important issues for consideration. It is a popular belief that prehistoric peoples had shorter life spans than we do today. If DISH is a phenomenon of old age and this Nubian population had a significantly high number of DISH cases, then did these Nubians generally live to advanced ages? Since the skeletons were not always complete, biological age could not be used accurately to reconstruct age of onset and demographic distributions of this phenomenon in these individuals. However, if we assume that DISH has neither changed its virulence nor the age of onset in the past 2,300 years, then this Nubian population had life expectancies that were long enough to yield high frequencies of severe manifestations of DISH. Some of the cases studied presented massive ossification even in the cervical area. Although DISH may start as early as age 43 (Julkunen et al., 1971), it is interesting that the prevalence definitely increases with age in an almost exponential manner. Why are females less affected by DISH? This is possibly due to female bone gracility and postmenopausal hormonal imbalances that decrease the amount of bone formation. Archaeologically and in modern clinical cases, males, are more affected with DISH than females. Therefore, upon finding a partial skeleton with much ossification due to DISH, if the sex cannot be inferred by standard physical anthropology procedures, 247 DISH IN NUBIANS then based on probability alone, the skeleton will most likely be a male. Hajkova et al. (1965) and Julkunen et al. (1971, 1975) have found that the frequency of DISH increases with the presence of diabetes mellitus and obesity. However, the association of DISH and diabetes mellitus is controversial. Resnick et al. (1978) and Rothschild (1985) among others argued that the studies showing association between DISH and diabetes mellitus are inconclusive because of the lack of standardized criteria for glucose tolerance in individuals above 40 years of age. Rothschild (1985, 1988) suggested that the presence of DISH may be advantageous, for instance, against neuroforamina1 narrowing. Waldron (1985) found that nearly 10% of the Medieval priest’s skeletons from Merton Priory had DISH. He attributed this high frequency to their gluttonous behavior. The high prevalence of DISH observed in the Nubians from Semna South, whether related to longevity o r obesity, needs further study. Based on the late age of onset for DISH and the hypothesis that diabetes and obesity may cause predisposition to DISH, Arriaza (1993) has postulated that DISH then should be common in the higher ranks of stratified prehistoric societies as compared to hunter-gatherer populations. Arriaza (1993) also theorized that DISH could be a response to an evolutionary trend of increasing longevity; that is, DISH is the biological response to excessive skeletal stress. Thus, skeletal hyperostosis of the spine and appendicular skeleton may benefit the individual by providing extra strength to support a weakened trunk and body, without a significant loss of mobility. In summary, DISH is not just a product of contemporaneous health disorders or modern human behavior; it has been present in the Old World for more than 2,000 years. As is the case in modern populations, DISH affected mostly males in ancient Nubia. DISH is associated with less destructive processes and much less pain than are the seronegative spondyloarthropathies. Patients with DISH complain of spinal stiffness and mild middle or lower back pain, but the condition is often discovered when the patient is being treated for other diseases typical of old age (Forestier and Rotes-Querol, 1950; Resnick et al., 1975). If DISH is the product of a trend toward increasing longevity; that is, if it is an age-adaptive phenomenon, then the frequency of DISH should decrease as we look back in time, and can be expected to continue increasing in future populations. LITERATURE CITED Armelagos GJ (1977) Disease in ancient Nubia. In D Landy (ed.):Culture, Disease, and Healing. 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